Effect of blue light on endogenous isopentenyladenine and endoreduplication during photomorphogenesis and de-etiolation of tomato (Solanum lycopersicum L.) seedlings

. 2012 ; 7 (9) : e45255. [epub] 20120925

Jazyk angličtina Země Spojené státy americké Médium print-electronic

Typ dokumentu časopisecké články, práce podpořená grantem

Perzistentní odkaz   https://www.medvik.cz/link/pmid23049779

Light is one of the most important factor influencing plant growth and development all through their life cycle. One of the well-known light-regulated processes is de-etiolation, i.e. the switch from skotomorphogenesis to photomorphogenesis. The hormones cytokinins (CKs) play an important role during the establishment of photomorphogenesis as exogenous CKs induced photomorphogenesis of dark-grown seedlings. Most of the studies are conducted on the plant model Arabidopsis, but no or few information are available for important crop species, such as tomato (Solanum lycopersicum L.). In our study, we analyzed for the first time the endogenous CKs content in tomato hypocotyls during skotomorphogenesis, photomorphogenesis and de-etiolation. For this purpose, two tomato genotypes were used: cv. Rutgers (wild-type; WT) and its corresponding mutant (7B-1) affected in its responses to blue light (BL). Using physiological and molecular approaches, we identified that the skotomorphogenesis is characterized by an endoreduplication-mediated cell expansion, which is inhibited upon BL exposure as seen by the accumulation of trancripts encoding CycD3, key regulators of the cell cycle. Our study showed for the first time that iP (isopentenyladenine) is the CK accumulated in the tomato hypocotyl upon BL exposure, suggesting its specific role in photomorphogenesis. This result was supported by physiological experiments and gene expression data. We propose a common model to explain the role and the relationship between CKs, namely iP, and endoreduplication during de-etiolation and photomorphogenesis.

Zobrazit více v PubMed

Schumacher K, Vafeados D, McCarthy M, Sze H, Wilkins T, et al. (1999) The Arabidopsis det3 mutant reveals a central role for the vacuolar H+-ATPase in plant growth and development. Gen Dev 13: 3259–3270. PubMed PMC

Cosgrove DJ (1981) Rapid suppression of growth by blue light: Occurrence, time course, and general characteristics. Plant Physiol 67: 584–590. PubMed PMC

Symons GM, Reid JB (2003) Interactions between light and plant hormones during de-etiolation. J Plant Growth Regul 22: 3–14.

Miller CO, Skoog F, Von Saltza MH, Strong FM (1955) Kinetin, a cell division factor from deoxyribonucleic acid. J Am Chem Soc 77: 1392–1393.

Werner T, Schmülling T (2009) Cytokinin action in plant development. Curr Opin Plant Biol 12: 527–538. PubMed

Perilli S, Moubayidin L, Sabatini S (2010) The molecular basis of cytokinin function. Curr Opin Plant Biol 13: 21–26. PubMed

Chory J, Aguilar N, Peto CA (1991) The phenotype of Arabidopsis thaliana det1 mutants suggests a role for cytokinins in greening. Symp Soc Exp Biol 45: 21–29. PubMed

Chin-Atkins AN, Craig S, Hocart CH, Dennis Es, Chaudhury MA (1996) Increased endogenous cytokinin in the Arabidopsis amp1 mutant corresponds with de-etiolation responses. Planta 198: 549–556. PubMed

Chory J, Reinecke D, Sim S, Washburn T, Brenner M (1994) A role for cytokinins in de-etiolation in Arabidopsis (det mutants have an altered response to cytokinins). Plant Physiol 104: 339–347. PubMed PMC

Vandenbussche F, Habricot Y, Condiff AS, Maldiney R, Vam Der Straeten D, et al. (2007) HY5 is a point of convergence between cryptochrome and cytokinin sigalling pathways in Arabidopsis thaliana. Plant J 49: 428–441. PubMed

Traas J, Hülskamp M, Gendreau E, Höfte H (1998) Endoreduplication and development: rule without dividing? Curr Opin Plant Biol 1: 498–503. PubMed

Vandenbussche F, Verbelen J-P, Vand Der Straeten D (2005) Of light and length: regulation of hypocotyl growth in Arabidopsis. BioEssays 27: 275–284. PubMed

Perrot-Rechenmann C (2010) Cellular responses to auxin: division versus expansion. In: Estelles M, Weijers D, Ljung K, Leyser O, editors. Auxin Signalling in CSH Perspectives in Biology. Cold Spring Harbor Laboratory Press, NY. doi:10.1101/cshperspect.a001446. PubMed DOI PMC

Boudolf V, Vlieghe K, Beemster GTS, Magyar Z, Torres Acosta JA, et al. (2004) The plant-specific cyclin-dependent kinase CDKB1;1 and transcription factor E2F-DPa control the balance of mitotically dividing and endoreduplicating cells in Arabidopsis. Plant Cell 16: 2683–2692. PubMed PMC

Verkest A, Weinl C, Inzé D, De Veylder L, Schnittger A (2005) Switching the cell cycle. Kip-related proteins in plant cell cycle control. Plant Physiol 139: 1099–1106. PubMed PMC

Dewitte W, Scofield S, Alcasabas AA, Maughan SC, Menges M, et al. (2007) Arabidopsis CYCD3 D-type cyclins link cell proliferation and endocycles and are rate-limiting for cytokin responses. Proc Natl Acad Sci USA 104: 14537–14542. PubMed PMC

Riou-Khamlichi C, Huntley R, Jacqmard A, Murray JAH (1999) Cytokinin activation of Arabidopsis cell division through a D-type cyclin. Nature 283: 1541–1544. PubMed

Sawhney VK (1997) Genetic male sterility. In: Shivanna KR, Sawhney VK, editors. Pollen biotechnology for crop production and improvement. Cambridge, UK: Cambridge University Press, 183–198.

Fellner M, Sawhney VK (2002) The 7B-1 mutant in tomato shows blue-light-specific resistance to osmotic stress and abscisic acid. Planta 214: 675–682. PubMed

Sheoran IS, Dumonceaux T, Datla R, Sawhney VK (2006) Anthocyanin accumulation in the hypocotyl of an ABA-over producing male-sterile tomato (Lycopersicon esculentum) mutant. Physiol Plantarum 127: 681–689.

Bergougnoux V, Hlavackova V, Plotzova R, Novak O, Fellner M (2009) The 7B-1 mutation in tomato (Solanum lycopersicum L.) confers a blue light-specific lower sensitivity to coronatine, a toxin produced by Pseudomonas syringae pv. tomato. J Exp Bot 60: 1219–1230. PubMed

Kvarnheden A, Yao J-L, Zhan X, O’Brien I, Morris BAM (2000) Isolation of three distinct CycD3 genes expressed during fruit development in tomato. J Exp Bot 51: 1789–1797. PubMed

Kurakawa T, Ueda N, Maekawa M, Kobayashi K, Kojima M, et al. (2007) Direct control of shoot meristem activity by a cytokinin-activating enzyme. Nature 445: 652–655. PubMed

Kuroha T, Tokunaga H, Kojima M, Ueda N, Ishida T, et al. (2009) Functional analysis of LONELY GUY cytokinin-activating enzymes reveal the importance of direct activation pathway in Arabidopsis. Plant Cell 21: 3152–3169. PubMed PMC

Mok DWS, Mok MC (2001) Cytokinin metabolism and action. Annu Rev Plant Physiol Plant Mol Biol 52: 89–118. PubMed

Werner T, Motyka V, Laucou V, Smets R, Van Onckelen H, et al. (2003) Cytokinin-deficient transgenic Arabidopsis plants show multiple developmental alterations indicating opposite functions of cytokinins in the regulation of shoot and root meristem activity. Plant Cell 15: 2532–2550. PubMed PMC

Galuszka P, Popelková H, Werner T, Frébortová J, Pospíšilová H, et al. (2007) Biochemical characterization of cytokinin oxidases/dehydrogenases from Arabidopsis thaliana expressed in Nicotiana tabacum L. J Plant Growth Regul. 26: 255–267.

Folta KM, Spalding EP (2001) Unexpected roles for cryptochrome 2 and phototropin revealed by high-resolution analysis of blue light-mediated hypocotyl growth inhibition. Plant J 26: 471–478. PubMed

Reid BR, Howell SH (1995) The functioning of hormones in plant growth and development. In PJ Davies, ed, Plant Hormones: Physiology, Biochemistry and Molecular Biology. Kluwer Academic Publishers, Dordrecht. The Netherlands, 4848–485.

Gendreau E, Traas J, Desnos T, Grandjean O, Caboche M, et al. (1997) Cellular basis of hypocotyl growth in Arabidopsis thaliana . Plant Physiol 114: 295–305. PubMed PMC

Gendreau E, Höfte H, Grandjean O, Brown S, Traas J (1998) Phytochrome controls the number of endoreduplication cycles in the Arabidopsis thaliana hypocotyl. Plant J 13: 221–230. PubMed

Jacqmard A, De Veylder L, Segers G, de Almeida Engler J, Bernier G, et al. (1999) Expression of CKS1At in Arabidopsis thaliana indicates a role for the protein in both the mitotic and the endorecuplication cycle. Planta 207: 496–504. PubMed

Lochmanová G, Zdráhal Z, Konečná H, Koukalová Š, Malbeck J, et al. (2008) Cytokinin-induced photomorphogenesis in dark-grown Arabidopsis: a proteomic analysis. J Exp Bot 59: 3705–3719. PubMed

Miyawaki K, Tarkowski P, Matsumoto-Kitano M, Kato T, Sato S, et al. (2006) Roles of Arabidopsis ATP/ADP isopentenyltransferases and tRNA isopentenyltransferases in cytokinin biosynthesis. Proc Natl Acad Sci USA 103: 16598–16603. PubMed PMC

Gajdošová S, Spíchal L, Kamínek M, Hoyerová K, Novák O, et al. (2011) Distribution, biological activities, metabolism, and the conceivable function of cis-zeatin-type cytokinins in plants. J Exp Bot doi:10.1093/jxb/erq457. PubMed DOI

Miyawaki K, Matsumoto-Kitano M, Kakimoto T (2004) Expression of cytokinin biosynthetic isopentenyltransferase genes in Arabidopsis: tissue specificity and regulation by auxin, cytokinin, and nitrate. Plant J 37: 128–138. PubMed

Hirose N, Takei K, Kuroha T, Kamada-Nobusada T, Hayashi H, et al. (2008) Regulation of cytokinin biosynthesis, compartmentalization and translocation. J Exp Bot 59: 75–83. PubMed

Inoue T, Higuchi M, Hashimoto Y, Seki M, Kobayashi M, et al. (2001) Identification of CRE1 as a cytokinin receptor from Arabidopsis. Nature 409: 1060–163. PubMed

Suzuki T, Miwa K, Ishikawa K, Yamada H, Aiba H, et al. (2001) The Arabidopsis sensor His-kinase, AHK4, can respond to cytokinins. Plant Cell Physiol 42: 107–113. PubMed

Choi J, Hwang I (2007) Cytokinin: perception, signal transduction and role in plant growth and development. J Plant Biol 5: 98–108.

Riefler M, Novak O, Strnad M, Schmulling T (2006) Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell 18: 40–54. PubMed PMC

Nisler J, Zatloukal M, Popa I, Doležal K, Strnad M, et al. (2010) Cytokinin receptor antagonists derived from 6-benzylaminopurine. Phytochemistry 71: 823–830. PubMed

Kusnetsov V, Landsberger M, Meurer J, Oelmuller R (1999) The assembly of the CAAT-box binding complex at a photosynthesis gene promoter is regulated by light, cytokinin, and the stage of the plastids. J Biol Chem 274: 36009–36014. PubMed

Cluis CP, Mouchel CF, Hardtke CS (2004) The Arabidopsis transcription factor HY5 integrates light and hormone signaling pathways. Plant J 38: /332–347. PubMed

Lee J, He K, Stolc V, Lee H, Figueroa P, et al. (2007) Analysis of transcription factor HY5 genomic binding sites revealed its hierarchical role in light regulation of development. Plant Cell 19: 731–749. PubMed PMC

Doležel J, Binarova P, Lucretti S (1989) Analysis of nuclear DNA content in plant cells by flow cytometry. Biol Plantarum 31: 113–120.

Doležel J, Sgorbati S, Lucretti S (1992) Comparison of three DNA fluorochromes for flow cytometric estimation of nuclear DNA content in plants. Physiol Plantarum 85: 625–631.

Novák O, Tarkowski P, Lenobel R, Dolezal K, Strnad M (2003) Quantitative analysis of cytokinins in plants by liquid chromatography/single-quadrupole mass spectrometry. Anal Chim Acta 480: 207–218.

Novák O, Hauserová E, Amakorová P, Doležal K, Strnad M (2008) Cytokinin profiling in plant tissues using ultra-performance liquid chromatography-electrospray tandem mass spectrometry. Phytochemistry 6: 2214–2224. PubMed

Poiré R, Wiese-Klinkenberg A, Parent B, Mielewczik M, Schurr U, et al. (2010) Diel time-courses of leaf growth in moncoto and dicot species: endogenous rhythms and temperature effects. J Exp Bot 61: 1751–1759. PubMed PMC

Nejnovějších 20 citací...

Zobrazit více v
Medvik | PubMed

Transcriptional regulation of male-sterility in 7B-1 male-sterile tomato mutant

. 2017 ; 12 (2) : e0170715. [epub] 20170208

Cytokinins Are Initial Targets of Light in the Control of Bud Outgrowth

. 2016 Sep ; 172 (1) : 489-509. [epub] 20160726

A subtracted cDNA library identifies genes up-regulated during PHOT1-mediated early step of de-etiolation in tomato (Solanum lycopersicum L.)

. 2016 Apr 18 ; 17 () : 291. [epub] 20160418

Spatio-temporal changes in endogenous abscisic acid contents during etiolated growth and photomorphogenesis in tomato seedlings

. 2015 ; 10 (8) : e1039213.

Identification of miRNAs with potential roles in regulation of anther development and male-sterility in 7B-1 male-sterile tomato mutant

. 2015 Oct 28 ; 16 () : 878. [epub] 20151028

DNA methylation and transcriptomic changes in response to different lights and stresses in 7B-1 male-sterile tomato

. 2015 ; 10 (4) : e0121864. [epub] 20150407

Endogenous abscisic acid promotes hypocotyl growth and affects endoreduplication during dark-induced growth in tomato (Solanum lycopersicum L.)

. 2015 ; 10 (2) : e0117793. [epub] 20150219

Najít záznam

Citační ukazatele

Nahrávání dat ...

    Možnosti archivace